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Table des matières / Contents

How much does grazing-induced heterogeneity impact plant diversity in wet grasslands?Benoît MARION, Anne BONIS & Jan-Bernard BOUZILLÉ ........................................................ 229–239

Spatial variability in growth-increment chronologies of long-lived freshwater mussels: Implications for climate impacts and reconstructionsBryan A. BLACK, Jason B. DUNHAM, Brett W. BLUNDON, Mark F. RAGGON & Daniela ZIMA ................................................................................................................................ 240–250

A multi-scale assessment of amphibian habitat selection: Wood frog response to timber harvestingSean M. BLOMQUIST & Malcolm L. HUNTER Jr. ...................................................................... 251–264

Stable isotope differentiation of freshwater and terrestrial vascular plants in two subarctic regionsHeather E. MILLIGAN, Troy D. PRETZLAW & Murray M. HUMPHRIES ............................. 265–275

Relationships among plant litter, fine roots, and soil organic C and N across an aridity gradient in northern Patagonia, ArgentinaAnalía L. CARRERA & Mónica B. BERTILLER ............................................................................ 276–286

Determinants of ground-dwelling spider assemblages at a regional scale in the Yukon Territory, CanadaJoseph J. BOWDEN & Christopher M. BUDDLE ......................................................................... 287–297

Effects of wildfire on endemic breeding birds in a Pinus canariensis forest of Tenerife, Canary IslandsEduardo GARCIA-DEL-REY, Rüdiger OTTO, José María FERNÁNDEZ-PALACIOS, Pascual GIL MUÑOZ & Luis GIL ....................................................................................................298–311

Climate sensitivity of thinleaf alder growth on an interior Alaskan floodplainDana R. NOSSOV, Roger W. RUESS & Teresa N. HOLLINGSWORTH ................................... 312–320

Winter habitat selection by caribou in relation to lichen abundance, wildfires, grazing, and landscape characteristics in northwest AlaskaKyle JOLY, F. Stuart CHAPIN III & David R. KLEIN .................................................................. 321–333

Short term response of small mammals and forest birds to silvicultural practices differing in tree retention in irregular boreal forestsMélanie-Louise Le BLANC, Daniel FORTIN, Marcel DARVEAU & Jean-Claude RUEL ...... 334–342

Erratum ....................................................................................................................................................................... 343

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17 (4): 387-393 (2010)

Ectotherms, by definition, have limited capacity for metabolic heat production. Consequently, reptiles faced with important diurnal and seasonal temperature fluctua-tions, such as in temperate areas, rely largely upon behav-ioural thermoregulation to maintain their body temperature (Tb) within a specific range. Because Tb dictates the rate of most physiological processes, behavioural thermoregulation is expected to provide numerous physiological benefits that could ultimately increase fitness (Huey & Slatkin, 1976; Huey, 1991). The most important effect of Tb on fitness is likely through modulation of the energy budget (Huey & Slatkin, 1976; Congdon, 1989). The amount of energy avail-able for growth or reproduction depends on many thermally sensitive processes, including metabolic rate (Gatten, 1974;

Kepenis & McManus, 1974), gut passage time (Parmenter, 1981; Avery et al., 1993), and ingestion rate (Kepenis & McManus, 1974; Avery et al., 1993). Thus, ectotherms have the potential to regulate their energy budget by behaviourally adjusting their Tb.

In reptiles, behavioural thermoregulation is common and includes behaviours such as selecting appropriate activ-ity times (Crawford, Spotila & Standora, 1983; Sinervo & Adolph, 1994) and thermal microenvironments (Huey et al., 1989; Adolph, 1990) as well as postural adjustments (Boyer, 1965; Seebacher, 1999). One of the most conspicu-ous thermoregulatory behaviours in ectotherms is basking: the exposure of at least part of the body to solar radiation while the animal is immobile. This behaviour is especially pronounced in freshwater turtles (Boyer, 1965). Indeed, many freshwater turtles commonly bask either at the sur-face of the water (aquatic basking) or completely emerged on substrates such as logs or rocks (atmospheric basking). Basking may serve multiple purposes, including enhancing

Estimating the energetic significance of basking behaviour in a temperate-zone turtle1

Grégory BULTÉ & Gabriel BLOUIN-DEMERS2, Department of Biology, University of Ottawa, 30 Marie-Curie,

Ottawa, Ontario K1N 6N5, Canada, gblouin@uottawa.ca

Abstract: Basking is a common thermoregulatory behaviour in many ectotherms, including reptiles. Because the key physiological processes affecting net energy retention (NER) are temperature dependent, ectotherms have the potential to modulate their energy budget by using basking behaviour. Many aquatic chelonians bask extensively. The energetic significance of basking is, however, largely unknown. We used biologging to measure the body temperature of free-ranging juvenile northern map turtles in Ontario, Canada. We measured the contribution of basking behaviour to the ability of turtles to reach their optimal body temperature for NER. We also used the predicted standard metabolic rate as a proxy to estimate the effects of basking on NER. Our results show that basking is essential for turtles to reach the optimal temperature for NER and suggest that basking behaviour allows turtles to increase their metabolic rate by 17.2 to 30.1%, which should translate into an even greater increase in NER. In addition, our results show that basking behaviour allows turtles to buffer the effects of climatic variations on their Tb and thus potentially on their energy budget. Collectively, our results suggest that basking behaviour has important ramifications for the energy budget, and by extension the fitness, of temperate-zone turtles.Keywords: basking behaviour, net energy retention, northern map turtle, standard metabolic rate.

Résumé : Se réchauffer au soleil est un comportement de thermorégulation commun chez de nombreux ectothermes, y compris les reptiles. Puisque les processus physiologiques clés ayant un impact sur la rétention d’énergie nette (REN) dépendent de la température, les ectothermes ont le potentiel de moduler leur budget énergétique en utilisant le comportement de réchauffement au soleil. De nombreux chéloniens aquatiques le font énormément. La signification énergétique du réchauffement au soleil est cependant très peu connue. Nous avons utilisé la biotélémétrie pour suivre la température corporelle de tortues géographiques juvéniles en milieu naturel en Ontario, Canada. Nous avons mesuré la contribution du comportement de réchauffement au soleil à la capacité des tortues d’atteindre leur température corporelle optimale pour la REN. Nous avons aussi utilisé le taux métabolique standard prédit comme indicateur pour évaluer les effets de ce comportement sur la REN. Nos résultats montrent que se réchauffer au soleil est essentiel pour les tortues afin d’atteindre la température optimale pour la REN et suggèrent que ce comportement permet aux tortues d’augmenter leur taux métabolique de 17,2 à 30,1 %, ce qui devrait se traduire en une augmentation encore plus grande de la REN. De plus, nos résultats montrent que ce comportement permet aux tortues de réduire les effets des variations climatiques sur leur Tb et ainsi potentiellement sur leur budget énergétique. Dans l’ensemble, nos résultats suggèrent que le comportement de réchauffement au soleil a des ramifications importantes pour le budget énergétique, et par extension sur la valeur adaptative, des tortues des régions tempérées.Mots-clés : comportement de réchauffement au soleil, rétention d’énergie nette, taux métabolique standard, tortue géographique.

Nomenclature: Le Sueur, 1817.

Introduction

1Rec. 2010-05-03; acc. 2010-09-09. Associate Editor: Patrick Gregory.2Author for correspondence.DOI 10.2980/17-4-3377

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vitamin metabolism (Ferguson et al., 2003), desiccating leeches (Ernst, 1971), and creating fevers to fight infection (Monagas & Gatten, 1983). In addition, in temperate-zone freshwater turtles, basking yields important thermal ben-efits (Grayson & Dorcas, 2004; Bulté & Blouin-Demers, 2010), suggesting that the energetic benefits would also be high. The energetic significance of this conspicuous bask-ing behaviour under natural conditions, however, remains largely unknown. In this study, we used biologging tech-nology to measure Tb in free-ranging northern map turtles (Graptemys geographica) at the northern limit of their range. Our primary objective was to estimate the ener-getic significance of basking behaviour. We determined the extent to which basking behaviour allows these turtles to maintain the estimated optimal Tb for energy assimilation. We estimated the relative increase in energy assimilation that is realized by basking. Our second objective was to determine if northern map turtles use their thermal environ-ment to maximize energy assimilation. We estimated the relative change in energy assimilation that turtles would experience if they were using all the available opportuni-ties to maintain their Tb within the optimal range for energy assimilation. Determining how much reptiles deviate from optimal thermoregulation offers insights on the cost of thermoregulation (Blouin-Demers & Weatherhead, 2001). Basking behaviour in chelonians is particularly interest-ing from a cost–benefit perspective because this behaviour occurs largely outside the water in many turtles, including the northern map turtle. Thus, basking behaviour is mutu-ally exclusive with other imperative activities, including foraging and mating, which both occur in water. As a third objective, we examined the effect of weather on basking behaviour and its energetic significance.

Methods

Biologging anD quantification of Basking Behaviour

We studied northern map turtles in Lake Opinicon, a small mesotrophic lake at the Queen’s University Biological Station 100 km south of Ottawa, Ontario, Canada. From mid April to early May 2005 and 2006, we captured northern map turtles at a communal hiberna-tion site. We surgically implanted temperature data log-gers (Thermocron iButton DS 2422; Dallas Semiconductor, Sunnyvale, California, USA) in the abdominal cavity of 14 juvenile females (9 in 2005 and 5 in 2006). Details of the anaesthetic and surgical procedures are provided by Edwards and Blouin-Demers (2007). The loggers recorded Tb every 25 min between May and October. Each turtle with an implanted logger was also equipped with a radio-trans-mitter (SI-2FT or SB-2FT; Holohil Systems, Carp, Ontario, Canada). The radio-transmitters were bolted to the rear mar-ginal scutes using stainless steel bolts. The combination of logger and radio-transmitter did not exceed 5% of the tur-tle’s mass. The fall or spring following logger implantation, we recaptured turtles to remove the transmitters and the loggers. Analyses were performed on Tb collected between May 15 and August 15 of each year.

The turtles used in this study were small and thus rapidly reached thermal equilibrium with water when submerged.

For instance, painted turtles of equal size to our juvenile northern map turtles (ca 400 g) need approximately 11 min to cool 10 °C when submerged in water (Costanzo, 1982). We thus assumed that any time a turtle’s Tb was above the maximum surface temperature of the water (Smax), the turtle was emerged and thus basking. We calculated hourly mean Tb for each individual. From the hourly means, we calculat-ed the percentage of time spent basking for each individual as the percentage of Tb measurements exceeding Smax. Thus, we obtained a single measurement of time spent basking per individual per year. In our calculation of the percentage of time spent basking, we excluded nighttime Tb measure-ments (1900 to 0700) because basking only occurs during the day. To obtain hourly measurements of Smax, we mea-sured water surface temperature at four locations in the lake with temperature loggers (Thermocron iButton DL 1922; Dallas Semiconductor, Sunnyvale, California, USA). We calculated hourly Smax as the maximum surface temperature of the 4 locations. The 4 locations were: 1 deep (7 m) open water site, 2 shallow open water sites (2–3 m), and 1 shal-low (1 m) marsh. These sites were selected to capture the range of possible surface temperatures in the lake.

stanDarD metaBolic rate anD net energy retention

We predicted the standard metabolic rate (SMR) of turtles from their Tb and used it as a proxy to estimate the effects of Tb on net energy retention (NER), the amount of energy available for growth and reproduction. Although predicting SMR from Tb is a linear transformation of Tb, SMR provides a better basis for interpreting the energetic implications of thermoregulation. Indeed, the physiological processes responsible for digestion, and thus energy reten-tion, depend on metabolic rate (Dubois, Blouin-Demers & Thomas, 2008; Dubois et al., 2009). In addition, below the optimal temperature for NER, NER increases faster with Tb than SMR (Dubois, Blouin-Demers & Thomas, 2008). Thus, we argue that SMR is a conservative proxy to deter-mine the relative change in NER with Tb as long as Tb is below the optimum temperature for NER (Dubois, Blouin-Demers & Thomas, 2008). Dubois, Blouin-Demers, and Thomas (2008) demonstrated that the optimal temperature (To) for NER matches the upper voluntary maximum Tb selected in a thermal gradient (Tset). In northern map turtles, Tset is between 28.7 and 32.5 °C (Bulté & Blouin-Demers, 2010). When predicting SMR from Tb, we excluded the Tb measurements above the upper bound of Tset (32.5 °C). Tb was above Tset only 2% of the time during the active season, indicating that at our latitude opportunities to maintain Tb above 32.5 °C are rare. We excluded these data because, in reptiles, SMR varies with Tb at a similar rate to food con-sumption or food passage only at Tb below To. Thus, at Tb above To the relationship between SMR and Tb no longer estimates the relationship between NER and Tb (Dubois, Blouin-Demers & Thomas, 2008).

As part of another study, we measured oxygen con-sumption in northern map turtles at 4 temperatures (14, 20, 26, and 32 °C) using open flow respirometry (see Bulté & Blouin-Demers, 2008 for details) in 6 juvenile females ranging in mass from 136 to 544 g and derived a predictive equation (Log V02 = –6.40 + 3.36*log Tb; R2 = 0.76) that

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we used to predict SMR from Tb. We performed our respi-rometry measurements in June and July 2006.

Determining the energetic significance of Basking anD the maximal net energy retention

To quantify the energetic significance of basking, for each individual we calculated the relative change in SMR that turtles would experience if they could not bask to raise their Tb above Smax. To predict the SMR of turtles unable to bask, we used the realized field Tb of the turtles (measured with the implanted loggers) and replaced all the mean hourly Tb that were above Smax by Smax for the same hour. We thus “removed” the basking events from the actual field Tb mea-surements and predicted SMR from these modified data.

To determine if map turtles were thermoregulating to maximize NER, we measured the Tb that turtles could have achieved in the lake and at basking sites. We mea-sured water temperature hourly with temperature loggers at 13 locations in Lake Opinicon. These locations were selected with the aim of representing the various habitats and depths available to turtles in Lake Opinicon. To deter-mine the body temperatures available to turtles when bask-ing, we used copper models of the same size and colour as juvenile females (Edwards & Blouin-Demers, 2007). The models were filled with water and placed on rocks and logs fully exposed to the sun because we wanted to capture the maximum available temperatures during basking. Model temperatures were also measured hourly with temperature loggers. Because the models were not used for the entire active season, we predicted temperature of models at bask-ing sites with predictive equations based on microclimate data collected at a weather station located on the shore of Lake Opinicon. We used multiple regressions with air tem-perature, solar radiation, wind speed, and wind direction to obtain equations predicting the temperatures of all models at all times (Blouin-Demers & Weatherhead, 2001). The pre-dictive equations explained most of the variation in model temperature (R2 > 0.81).

To generate the thermal profile of a turtle maximiz-ing NER for every hour during the active season, we used the available temperature (water temperature or physical model temperature) closest to Tset as our measure of Tb. Thus, when all available temperatures were below Tset, we used the maximum available temperature as Tb, and when available temperatures were above or within Tset for growth, we used the upper limit of Tset (32.5 °C) as Tb. As before, to determine the Tb of turtles in the absence of basking behaviour, we replaced all the Tb measurements above Smax with the mean surface temperature of the lake for the cor-responding hour.

Results

Mean plastron length of turtles at recovery of the log-gers was 138 mm (range: 123 to 151 mm), and there was no difference in percentage increase in plastron length between 2005 and 2006 (t-test: t12 = 0.47, P = 0.65, Table I). The per-centage of mass uptake, however, was greater in 2005 than in 2006 (t-test: t12 = 2.52, P = 0.03, Table I). The average mass at recovery in 2005 was 467 g (range: 384 to 558 g) compared to 379 g (range: 298 to 495 g) in 2006 (Table I).

The mean surface temperature of the lake was higher in 2005 than in 2006, except in May (Figure 1). Overall, juvenile female northern map turtles were able to raise Tb substantially above Smax (Figure 2). The percentage of Tb measurements above Smax during daylight hours was

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taBle i. Mean (range) mass and length at implantation and recovery of juvenile female northern map turtles (n = 14 individuals) from Lake Opinicon, Ontario, Canada in 2005 and 2006.

2005 2006

Mass (g) Implantation 325 (260–376) 299 (250–376) Recovery 467 (384–558) 379 (298–495)Plastron length (mm) Implantation 127 (123–134) 121 (114–136) Recovery 141 (132–151) 132 (123–148)

figure 1. Monthly mean surface water temperature in Lake Opinicon, Ontario, Canada in 2005 and 2006.

figure 2. Mean hourly body temperature (2005 and 2006 combined) of juvenile female northern map turtles (n = 14 individuals) from Lake Opinicon, Ontario, Canada. Hourly mean maximum (n = 4 sites) water surface temperature is indicated by the dashed line. Error bars indicate standard error.

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higher in 2006 than in 2005 (t-test; t11 = –2.26, P = 0.04). In 2005, 43.6% (range: 36.7 to 51.5%) of the Tb measure-ments exceeded Smax, compared to 53.0% (range: 40.0 to 67.8%) in 2006. In 2005, Smax was within Tset 28% of the daylight hours compared to 5.4% in 2006. The percentage of Tb measurements within Tset during daylight hours was higher in 2005 than in 2006 (t-test; t11 = 3.04, P = 0.01). In 2005, 24% (range: 17.8 to 30.8%) of the Tb measurements were within Tset, compared to 18% (range: 14 to 20.5%) in 2006 (Figure 3). When Tb could not exceed Smax (i.e., we removed basking events by substituting Smax for Tb when Tb exceeded Smax), Tb measurements within Tset during daylight hours declined to 5.0% (range: 3.7 to 6.6%) in 2005 and to 0.1 % (range: 0 to 0.3%) in 2006 (Figure 4). The available body temperatures sampled throughout the lake indicated that turtles would have been able to maintain their Tb within Tset 50.2 % of the daylight hours in 2005 and 41.2% of the daylight hours in 2006.

In 2005, 82% of the Tb measurements within Tset of map turtles occurred when Tb exceeded Smax (i.e., when turtles were basking) compared to 99% in 2006. The SMR predicted from the actual field Tb of map turtles was higher

than the SMR predicted from the modified data in which we removed basking by preventing Tb from exceeding Smax. The relative decrease in SMR was greater in 2006 than in 2005. When Tb could not exceed Smax (i.e., when we removed the basking events), predicted SMR of map turtles decreased by 20.2% (range: 17.1 to 26.0%) in 2005 and by 27.7% (range: 21.2 to 30.2%) in 2006. Always selecting the available temperatures that maximize NER (perfect thermo-regulation with respect to energy acquisition) would trans-late to a mean increase in predicted SMR of 33.2% (range: 24.4 to 41.9 %) compared to the SMR experienced by map turtles in Lake Opinicon.

Discussion

The main objective of our study was to quantify the energetic significance of basking behaviour in a temperate-zone turtle. Our results suggest that basking behaviour deeply affects the energy budget of northern map turtles. We showed that basking behaviour is essential for juvenile female northern map turtles to reach their optimum tem-perature for NER. Indeed, turtles were basking at least 91% of the time (both years combined) when Tb was within Tset.

figure 3. Frequency distribution of estimated body temperatures of juvenile female northern map turtles (n = 14) in Lake Opinicon, Ontario, Canada between the hours of 0700 and 1900 in 2005 and 2006. The dashed lines indicate the estimated optimal temperature range for net energy retention.

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In addition, if map turtles had not been able to bask they would have sustained decreases in SMR ranging from 17.2 to 30.1%. Such decreases in SMR would conceivably be accompanied by an even greater decrease in NER because the Q10 for NER is typically greater than for SMR (Dubois, Blouin-Demers & Thomas, 2008).

Although basking behaviour clearly brings some important energetic benefits, our estimates indicate that juvenile northern map turtles are not thermoregulating to the maximum extent possible to increase NER. A hypotheti-cal turtle maximizing NER via perfect thermoregulation would be able to increase its SMR by 33.2% according to our estimates. The disinclination of turtles to maximize NER in their thermal environment could reflect limited thermoregulation opportunities, a trade-off between ther-moregulation and other activities, or a trade-off between competing physiological processes. Basking competition (Lovich, 1988) seems an unlikely explanation for the dis-inclination of map turtles to maximize NER because map turtles commonly bask on top of one another and basking

sites do not appear to be limited in our study area (G. Bulté, pers. observ.). We did not measure the availability of the achievable Tb in the environment, so we cannot rule out the possibility that turtles could not thermoregulate to maxi-mize NER because of limited opportunities to bask, but as explained above this seems unlikely given the availability of basking sites in Lake Opinicon. We did measure achievable Tb in environments that were seemingly broadly available to turtles, however.

A more probable explanation for imperfect thermo-regulation is that turtles are not maximizing NER through basking due to a trade-off between the costs and benefits of thermoregulation (Huey & Slatkin, 1976). Basking behav-iour occurs largely out of the water in map turtles. This behaviour thus conflicts with other activities, including for-aging. In our modelling of the maximal NER that could be achieved through perfect thermoregulation, we assumed that foraging time only represents a minor portion of map turtle time budget and that Tb is the limiting factor on NER. We felt this was reasonable because foraging time is likely short

figure 4. Frequency distribution of estimated juvenile female northern map turtle (n = 14) body temperatures when basking is excluded in Lake Opinicon, Ontario, Canada between the hours of 0700 and 1900 in 2005 and 2006. The dashed lines indicate the estimated optimal temperature range for net energy retention.

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relative to processing time in freshwater turtles (Congdon, 1989). For instance, the predicted digestive turnover rate at 27 °C in the painted turtle (Chrysemys picta) is 42 h (Parmenter, 1981). At our study site, the density of banded mystery snails (Viviparus georgianus) and zebra mus-sels (Dreissena polymorpha), the main prey items of map turtles, averaged 35 and 2592 individuals·m–2, respectively (Bulté, Gravel & Blouin-Demers, 2008). Thus, the time required for turtles to fill their digestive tract is likely much shorter than the digestive turnover. During daylight hours, map turtles spend on average at least 46.0% of their time basking. The high proportion of the time budget devoted to basking supports the idea that Tb is an important bottleneck on NER. To maximize NER via thermoregulation, however, map turtles would have to be basking on average 73.8% of the time during daylight hours. Such an important time investment in basking could conceivably impede forag-ing time or other activities. In addition, although NER is likely the most important benefit of basking in turtles, other key physiological processes, such as immunological pro-cesses, may be maximized at different Tb than NER. Thus, the realized Tb of map turtles may also represent a trade-off between multiple optima (Angilletta, Niewiarowski & Navas, 2002). Dubois et al. (2009) performed the same analysis with wood turtles at similar latitude. They found that if wood turtles were using the thermal environment to maximize NER, they would increase their NER by up to 93%. This interspecific difference in potential NER sug-gests that costs of thermoregulation are lower in northern map turtles than in wood turtles.

We found marked differences in basking behaviour and its energetic significance between the 2 y of the study. In the cooler year (2006), turtles spent nearly 10% more time basking during the day, but their Tb was 11% less often within Tset than in the warmer year (2005). The mass increase of turtles was on average 20% higher in the warmer year. Thus, according to our estimates, turtles plausibly experienced lower NER due to lower Tb in the cooler year. The mean predicted SMR was 13% lower in the cooler year. These results support the idea that weather is a strong deter-minant of the energy budget of reptiles (Sinervo & Adolph, 1994; Angilletta, 2001). Nevertheless, basking behaviour seemingly allows turtles to buffer the effects of weather on NER. Indeed, the predicted SMR would have been 22% lower in the cooler year, as opposed to 13%, without the possibility of basking.

Collectively our data suggest that basking behaviour has considerable energetic implications. Basking behaviour has important ramifications for the energy budget, and by extension the fitness, of temperate-zone turtles. Indeed, NER dictates the energy available for growth and reproduc-tion. These results were not entirely unexpected, because the thermal significance of basking behaviour in temper-ate-zone turtles has already been established (Grayson & Dorcas, 2004; Bulté & Blouin-Demers, 2010). Yet, to our knowledge the energetic significance of basking had never been quantified. In addition, our results show that basking behaviour allows turtles to buffer the effects of seasonal variation in environmental temperature on their Tb, and thus by extension on their energy budget.

Acknowledgements

For their able help in the field, we are grateful to B. J. Howes, E. Ben-Ezra, S. Duchesneau, L. Patterson, C. Verly, and M.-A. Gravel. We are indebted to the Queen’s University Biological Station and its staff for logistical support. This study was funded by the Natural Sciences and Engineering Research Council of Canada, the Canada Foundation for Innovation, Parks Canada, le Fonds québécois sur la nature et les technologies, and the University of Ottawa through grants to G. Blouin-Demers and G. Bulté. Our procedures were approved by the Animal Care Committee at the University of Ottawa (protocol BL-179), and our scientific collector’s permit (authorization no: 1045605) was pro-vided by the Ontario Ministry of Natural Resources.

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